All but five of the N-terminal 23 residues of the HA2 domain of the influenza virus glycoprotein hemagglutinin (HA) are strictly conserved across all 16 serotypes of HA genes. The structure and function of this HA2 fusion peptide (HAfp) continues to be the focus of extensive biophysical, computational, and functional analysis, but most of these analyses are of peptides that do not include the strictly conserved residues Trp21-Tyr22-Gly23. Our heteronuclear triple resonance NMR study of full length HAfp of sero subtype H1, solubilized in dodecylphosphatidyl choline (DPC), previously revealed a remarkably tight helical hairpin structure, with its N-terminal alpha-helix (Gly1-Glu11) packed tightly against its second alpha-helix (Trp14-Gly23), with six of the seven conserved Gly residues at the interhelical interface. The seventh conserved Gly residue in position 13 adopts a positive phi angle, enabling the hairpin turn that links the two helices. The structure was found to be stabilized by multiple aliphatic interhelical CaH to C=O hydrogen bonds, characterized by strong interhelical HN-Ha; and Ha-Hb NOE contacts. New evidence for an additional stabilizing force of this hairpin structure has now been identified, namely a strong charge dipole interaction between the N-terminal Gly1 amino group and the dipole moment of helix 2. pH titration of the amino-terminal 15N resonance, using a novel methylene-TROSY based 3D NMR experiment, and observation of Gly1 13C' show a strongly elevated pK value of 8.8, considerably higher than expected for an N-terminal amino group in a lipophilic environment. Chemical shifts of three C-terminal carbonyl carbons of helix 2 titrate with the protonation state of Gly1-N, indicative of a close proximity between the N-terminal amino group and the axis of helix 2, thereby providing an optimal charge-dipole stabilization of the antiparallel hairpin fold. pK values of the side chain carboxylate groups of Glu11 and Asp19 are higher by about one and 0.5 unit, respectively, than commonly seen for solvent-exposed side chains in water-soluble proteins, indicative of dielectric constants of epsilon&#61472; = 30 (Glu11) and epsilon&#61472;= 60 (Asp19), which places these groups in the headgroup region of the phospholipid micelle. Biological membranes present a highly fluid environment and integration of proteins within such membranes is itself highly dynamic: proteins diffuse laterally within the plane of the membrane, and rotationally about the normal vector of this plane. We have found that whole-body motions of proteins within a lipid bilayer can be determined from NMR 15N relaxation rates collected for different size bicelles. The importance of membrane integration and interaction is particularly acute for proteins and peptides that function on the membrane itself, as is the case for pore-forming and fusion-inducing proteins. For the influenza hemagglutinin fusion peptide, which lies on the surface of membranes and catalyzes the fusion of membranes and vesicles, we find large-amplitude, rigid-body wobbling motions on the nanosecond timescale relative to the lipid bilayer. This behavior complements prior analyses where data were commonly interpreted in terms of a static oblique angle of insertion for the fusion peptide with respect to the membrane. Quantitative disentanglement of the relative motions of two interacting objects by systematically varying the size of one is applicable to a wide range of systems beyond protein-membrane interactions. At low pH (4.0) there is evidence in the NMR spectrum of the transient presence of another lowly populated activated state. By linking relaxation and chemical shift effects, we have found evidence that this activated state is similar to a state that is highly populated in the G8A mutant of the peptide. This latter structure is found to exist as an equilibrium between 20% of the original hairpin structure, and for the remainder of the time samples open, more extended structures without direct interhelical contacts. These extended structures are sufficient in size to span the membrane, and may be involved in formation of the actual fusion pore. The results of our study differ relative to those of earlier studies that focused on a shorter, 20-residue synthetic version of the fusion peptide. This 20-residue peptide was reported to adopt an open boomerang structure that differs significantly from the closed helical-hairpin structure we found for the first 23 residues of the HA2 sequence. By studying shorter versions of the fusion peptide, we found that the absence of several key interactions involving residues 21-23, that stabilize the closed, helical-hairpin structure, causes the 20-residue peptide to be in a dynamic equilibrium between closed and open states, adopting a ca. 11% population of the former when solubilized by DPC micelles. Peptides shorter than 20 residues have even fewer interactions to stabilize a helical hairpin fold, resulting in a vanishing hairpin population. Considering the conserved nature of hairpin-stabilizing interactions across all serotypes, and the minimum of 20 residues needed for membrane fusion, we postulate that the closed state plays an essential role in the fusion process. However, opening of this hairpin structure appears essential to the formation of a membrane pore at the final stage of the fusion process.